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Water Stress and Abscisic Acid Treatments Induce the CAM Pathway in the Epiphytic Fern Vittaria Lineata (L.) Smith

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Water Stress and Abscisic Acid Treatments Induce the CAM Pathway in the Epiphytic Fern Vittaria Lineata (L.) Smith DOI: 10.1007/s11099-014-0047-4 PHOTOSYNTHETICA 52 (3): 404-412, 2014 Water stress and abscisic acid treatments induce the CAM pathway in the epiphytic fern Vittaria lineata (L.) Smith B.D. MINARDI+, A.P.L. VOYTENA, M. SANTOS, and Á.M. RANDI Plant Physiology Laboratory, Department of Botany, Federal University of Santa Catarina, Florianópolis, SC– 88049-900, CP 476, Brazil. Abstract Among various epiphytic ferns found in the Brazilian Atlantic Forest, we studied Vittaria lineata (L.) Smith (Polypodiopsida, Pteridaceae). Anatomical characterization of the leaf was carried out by light microscopy, fluorescence microscopy, and scanning electron microscopy. V. lineata possesses succulent leaves with two longitudinal furrows on the abaxial surface. We observed abundant stomata inside the furrows, glandular trichomes, paraphises, and sporangia. We examined malate concentrations in leaves, relative water content (RWC), photosynthetic pigments, and chlorophyll (Chl) a fluorescence in control, water-deficient, and abscisic acid (ABA)-treated plants. Plants subjected to drought stress (DS) and treated by exogenous ABA showed significant increase in the malate concentration, demonstrating nocturnal acidification. These findings suggest that V. lineata could change its mode of carbon fixation from C3 to the CAM pathway in response to drought. No significant changes in RWC were observed among treatments. Moreover, although plants subjected to stress treatments showed a significant decline in the contents of Chl a and b, the concentrations of carotenoids were stable. Photosynthetic parameters obtained from rapid light curves showed a significant decrease after DS and ABA treatments. Additional key words: chlorophyll fluorescence; malate; morphoanatomy; photosynthetic pathway; pigments. Introduction Ferns are extensively distributed worldwide. These plants both land and water. They are climbers, thrive amid rocks, have developed remarkable adaptations in extreme envi- and they can be also epiphytes or hemiepiphytes, ranging ronments, being found in widely different habitats from tiny plants of a few millimeters to long, arborescent (Rathinasabapathi 2006). Many species are cosmopolitan forms reaching 20 m (Tryon and Tryon 1982). The and preferentially live in the tropical regions of the world, epiphytes comprise approximately 10% of the vascular especially in humid and shady forests (Rathinasabapathi flora (Kress 1986). They are found almost exclusively in 2006). Prado (2003) found approximately 13,000 species tropical forests, where they make up to 25% of species of ferns and lycophytes worldwide, out of which more (Nieder et al. 2001). According to Madison (1977), than 1,200 belong to Lycophyta and about 11,500 to epiphytic plants do not have direct connections with the Monilophyta (Pryer et al. 2004). ground. They only use phorophytes as a support, not as a Ferns are a very important group of plants which show source of nutrients. In an ecological context, epiphytism is well diversified ecological aspects. They have adapted to an interaction between plants in which the epiphytic ——— Received 3 June 2013, accepted 17 December 2013. +Corresponding author; fax: 0055-48-37218535; e-mail: [email protected]. Abbreviations: A – scaling constant for the height of the light curve; ABA – abscisic acid; AL – actinic light; Car – carotenoids; DM – dry mass; DS – drought stress; ETR – electron transport rate; ETRmax – maximum electron transport rate; FM – fresh mass; F0 – minimum fluorescence; Fm – maximum fluorescence; Fv – variable fluorescence; Fm'– minimum fluorescence of a light-adapted leaf; F' – fluorescence yield of a light-adapted leaf; FLM – fluorescence microscopy; Fv/Fm – maximum photochemical efficiency of PSII; I – irradiance; Iopt – optimal irradiance for the saturation of photosynthesis; kw – scaling constant for the x-axis of the light curve; LM – light microscopy; OAA – oxaloacetic acid; PAM – pulse-amplitude modulation; P – photosynthesis; PEG – polyethylene glycol; PEPC – phosphoenolpyruvate carboxylase; RLC – rapid light curve; RWC – relative water content; SEM – scanning electron microscopy; SL – saturating light pulses; TM – turgid mass; ФPSII – actual photochemical efficiency of PSII. Acknowledgments: The first authors would like to acknowledge CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) for the scholarship (Rede em Epífitas de Mata Atlântica: Sistemática, Ecologia E Conservação, CAPES, PNADB, 2009). Á.M. Randi and M. Santos would like to acknowledge CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the research grants. 404 CAM PATHWAY IN VITTARIA LINEATA plant is dependent only on the substrate supplied by the 1983, Sinclair 1984, Ravensberg and Hennipmam 1986, host plant (phorophyte); otherwise, they obtain nutrients Rut et al. 2008). Increase in titratable acidity was found in directly from atmospheric moisture, without emitting Dictymia J. Sm (Griffiths 1989) and V. lineata (Carter and haustorium structures (Bennett 1986). Vittaria lineata (L.) Martin 1994). Recently, Martin et al. (2005) showed some Smith (Pteridaceae) is an epiphytic fern found in the evidence of the CAM pathway in Vittaria flexuosa Fée and Brazilian Atlantic Forest. It is an exclusively epiphytic Anetium citrifolium (L.) Splitg., but not in V. lineata. On species without petioles and presenting laminar leaf the other hand, Martin et al. (2005) suggest the CAM (10–50 cm), simple, pendulous; linear sori is in a row pathway for V. flexuosa and A. citrifolium, which may be between the rachis and the margin and monolete spores also a sporadic phenomenon in V. lineata, thus explaining (Tryon and Tryon 1982, Smith et al. 2006). Known the disparity between the findings of Martin et al. (2005) popularly as "shoe cord fern", this species grows and those of Carter and Martin (1994). However, the preferentially in damp woods as epiphytes on tree trunks titratable acidity may not be enough to establish the or in the canopy (Tryon and Tryon 1982). Based on its presence of the CAM pathway because substances other beauty and hardiness, it is an ornamental plant widely used than malate may influence the pH of the samples. Zotz and in gardens. Ziegler (1997) studied the occurrence of CAM in different The epiphytism favors the capture of light radiation, vascular epiphytes in a central Panamanian forest via 13C but limits the availability of water. The CAM pathway is isotope and they verified C3 metabolism in V. lineata. one of the most important adaptations of some epiphytic CAM was initially verified in the epiphytic fern ferns to water deficit. It enables CO2 assimilation at Vittaria lineata (L.) Smith by Carter and Martin (1994), increased water deficiency and high irradiance stress but the presence of this pathway in V. lineata has never (Benzing 1986, 1990; Kluge et al. 1989). In plants that been confirmed (Zotz and Ziegler 1997, Martin et al. show the CAM pathway, CO2 enters the mesophyll leaf 2005). We hypothesized that V. lineata could change its tissue through open stomata predominantly at night and is mode of carbon fixation from C3 to the CAM pathway in fixed in the reaction catalyzed by phosphoenolpyruvate response to water deficit and exogenous application of carboxylase (PEPC) in the cytosol. The oxaloacetate ABA. Therefore, this study aimed to analyze the effects of (OAA) resulting from PEPC activity is reduced to malic water deficit and ABA application on relative water acid, which is accumulated in the vacuole at nighttime content (RWC), photosynthetic pigments, rapid light (Lüttge 1993, Nimmo 2000). curves, and fluctuations in the malate contents in leaves in In the Polypodiaceae, the CAM pathway was found in order to evaluate the physiological adaptations of five species of Pyrrosia and in Platycerium bifurcatum V. lineata to stress. (Hew and Wong 1974, Wong and Hew 1976, Winter et al. Materials and methods Plant collection: Plants of Vittaria lineata (L.) Smith were they were irrigated with Hoagland's solution (20%, v/v) collected from the natural habitat in the Environmental (Hoagland and Arnon 1938). After the acclimation period Conservation Unit “Desterro” (UCAD), located in the of at least six months, the plants were divided into three northwestern part of the island of Florianópolis, Santa groups, each subjected to a different conditions: (1) control Catarina, Brazil (27°31'50''S, 48°30'44''W, an area of 495 plants irrigated daily for two weeks, (2) plants subjected to ha, which is about 1% of the area of the island). The unit DS for a period of one week (without irrigation), and (3) is managed by the Federal University of Santa Catarina plants irrigated 5 times a week with a solution of 10 µM (UFSC), Florianópolis, Santa Catarina, SC, Brazil. ABA for a period of 15 d. Plant acclimation: Plants were transported to the green- Structural analysis of leaves: From the leaves in vivo, we house of the Botany Department of the Federal University cut freehand cross sections, both longitudinal and para- of Santa Catarina, where they grew for a minimum of six dermic, with a razor blade, using polystyrene as support months. The plants were placed in brackets on the walls. material. These sections were placed on a glass slide with During the testing period, the daily temperature of the water and covered with a cover slip. Histochemical stain- greenhouse varied between 20–30°C, and at night, it was ing was carried out using Lugol's solution for identification kept around 15°C. The relative humidity
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